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Macro- and microelement contents in fruiting bodies of wild mushrooms from the Notecka forest in west-central Poland
Food Chemistry Food Chemistry 92 (2005) 499–506 www.elsevier.com/locate/foodchem
Macro- and microelement contents in fruiting bodies of wild mushrooms from the Notecka forest in west-central Poland Maria Rudawska *, Tomasz Leski Institute of Dendrology, Polish Academy of Sciences, 5 Parkowa Str., 62-035 Ko´rnik, Poland Received 26 April 2004; received in revised form 17 August 2004; accepted 17 August 2004
Abstract Fruiting bodies of wild mushrooms and forest soil samples were collected and analyzed for macro- (N, P, K, S, Ca, Mg) and microelement (Al, Zn, Fe, Mn, Cd, Pb) contents in pine stands of the Notecka Forest in west-central Poland. Elements were determined by atomic absorption spectrometry in 160 samples of 8 fungal species and 15 underlying soil samples. Macro- and microelement contents in soil were low and characteristic of the poor and acidic sandy soils of the Polish lowlands not influenced by industrial pollution. In fruiting bodies, the highest mean concentration of macroelements (dry mass basis) was found for N (40.0 g kg 1), followed by K (33.0 g kg 1), P (5.4 g kg 1), S (2.2 g kg 1), Ca (1.0 g kg 1) and Mg (0.7 g kg 1). All macroelements (except for Ca) were concentrated in considerably higher levels in the fruiting bodies than in the forest soil. Nitrogen, P, K, S and Mg were preferably translocated into the cap rather than the stipes. Calcium, however, was often found in higher concentration in stipes than in caps. The mean microelement concentrations, across all tested fungi, were in the following order: Al > Zn > Fe > Mn > Pb > Cd. Microelements showed different distributions, depending on the part of the fruiting body. Some were more concentrated in the caps and some in stipes and distributions varied among species. Xerocomus badius is the most often harvested edible mushroom in the Notecka Forest. Pb and Cd distributions in fruiting bodies of this mushroom were evaluated in order to assess health risks to consumers. The estimated dietary exposures to Pb and Cd for consumers of this mushroom were in excess of guidelines on safe exposures. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Essential elements; Trace metals; Ectomycorrhizal fungi; Edible mushrooms
1. Introduction Fungi are important organisms in nature and are present almost everywhere. There are numerous species of wild mushrooms and many are edible. Mushrooms do not constitute a significant portion of the human diet; however, the consumption of wild and cultivated mushrooms continues to increase in many countries (e.g., Alonso, Garcia, Pe´rez-Lo´pez, & Melgar, 2003; Demirbasß, 2000; Falandysz et al., 2001; Kalacˇ & Svoboda, 2000; Latiff, Daran, & Mohamed, 1996; Longvah & *
Corresponding author. Tel.: +48 61 8170033/8170166; fax: +48 61 8170166. E-mail address: [email protected] (M. Rudawska). 0308-8146/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodchem.2004.08.017
Deosthale, 1998; Manzi, Aguzzi, & Pizzoferrato, 2001; Sanmee, Dell, Lumyong, Izumori, & Lumyong, 2003). Many common mushrooms, for example, Amanita, Suillus, Xerocomus, Lactarius, Russula, Leccinum and Paxillus, are ectomycorrhizal (ECM). External mycelia of ECM fungi (vegetative phase) spread below-ground around trees, acquiring water and minerals from the soil to benefit trees in symbiotic associations (Smith & Read, 1997). Fungal fruiting bodies are also connected to host roots through mycelia which transport carbohydrates necessary for their development. During rainy seasons, the fruiting bodies of ECM fungi can be seen in forests. They represent a visible by-product of ECM mycelia and function as reproductive structures. The chemical composition and nutritional quality of different wild
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and cultivated mushroom species have been studied (Aletor, 1985; Alofe, Odeyemi, & Oke, 1996; Dı´ez & Alvarez, 2001; Kreula, Saarivirta, & Karanko, 1976; Longvah & Deosthale, 1998; Manzi et al., 2001; Manzi, Gambelli, Marconi, Vivanti, & Pizzoferrato, 1999; Senatore, Dini, & Marino, 1988; Tshinyangu, 1996). Besides water (85–95% f.w.), carbohydrates (39.9% d.w.), proteins (17.5% d.w.) and low contents of lipids (2.9% d.w.) (Latiff et al., 1996), the wide variety and abundance of minerals are the most characteristic features of ECM fruiting bodies. Macro- and microelements present in the environment are to different extents accumulated by ECM vegetative mycelia and in the ECM fruiting bodies (Harmon, Sexton, Caldwell, & Carpenter, 1994; Kreula et al., 1976; Sanmee et al., 2003; Vogt & Edmonds, 1980). Several studies have been carried out on the trace element contents in fruiting bodies of the wild-growing edible mushrooms in Poland. The major publications consider levels of heavy metals in groups of mushrooms comprised of various species and collected in highly polluted or control sites (Falandysz, Danisiewicz, & Bona, 1994; Grzybek & Janczy, 1990; Malinowska, Szafer, & Falandysz, 2004; Turnau, 1991). Data on the general patterns of macro- and microelement accumulations in fruiting bodies of wild, ECM fungi in Poland are scarce and limited to a few sites in the Pomorskie Voivodeship in northern Poland (Falandysz et al., 2001; Malinowska et al., 2004). Poland is the largest producer of wild mushrooms in Europe and the largest European exporter of edible mushrooms. Commercial harvesting of mushrooms in Poland has a long tradition. A total of 1.71, 3.28, and 2.38 million kg of mushrooms were purchased by the food industry in 2000, 2001 and 2002, respectively (Statistical Yearbook – Forestry, 2003). Of this total, around half (depending on the year) originated from the Notecka Forest situated in west-central Poland. This study was initiated to (1) evaluate macro- and microelement contents in fruiting bodies of wild grown, mostly edible ectomycorrhizal fungi collected in the Notecka Forest region, and (2) determine which toxic metals were accumulated in higher concentrations in fruiting bodies of a frequently harvested and eaten mushroom, X. badius, in order to assess the health risks to consumers.
2. Materials and methods
homogeneous, both with regard to landscape formation and forest vegetation. Soils of this area are influenced mostly by planting haplic podzol and inland dunes with Scots pine (Pinus sylvestris) as the dominant tree species (95%). The Notecka Forest is situated far away from the acute sources of industrial pollution and is considered to be one of the most important centres for commercial harvesting of mushrooms in Poland. 2.2. Mushrooms and soil sampling The fruiting bodies of eight mushrooms species, namely Amanita rubescens, Lactarius deliciosus, L. rufus, Leccinum scabrum, Paxillus involutus, Suillus luteus, Xerocomus badius, and X. chrysenteron, were selected for this study. All these mushrooms have been consumed; however, the edibility of P. involutus and L. rufus is problematic (see Section 3). Fruiting bodies (2–4 fruiting bodies of each species per site) collected in five different areas of the Notecka Forest were divided into the cap and stipe, rinsed in deionized water to remove adhering particles, dried at 60 °C for 48 h, and ground in an automatic mortar; 160 samples of fleshy fruiting bodies (80 caps and 80 stipes) were analyzed. In addition to the mushroom collection, 15 soil samples of the upper forest soil horizon (0–10 cm, after removing the surface layer of organic detritus) were also collected at appropriate sampling places. 2.3. Chemical analysis Soil samples and milled fruiting bodies, of approximately 2.5 g d.w. each, were digested in a mixture of spectrally pure concentrated acids: HNO3 and HClO4 in a proportion of 4:1 (v:v) and diluted with bi-distilled water to make 25 ml. Nitrogen was analyzed by the micro-Kjeldahl method. The rest of the macroelements, aluminium, and heavy metals (Mn, Fe, Zn, Cd and Pb), were measured by atomic absorption spectroscopy (Varian 220 FS) with atomization in an air-acetylene flame. The accuracy of the analyses was checked against standard reference material, namely pine needles SRM 1575 and tomato leaves SRM 1573a (National Institute of Standards and Technology). Detection limit values of microelements, in microgrammes per litre were found to be 1.3 for Al, 0.05 for Mn, 0.11 for Fe, 0.02 for Zn, 0.02 for Cd, and 0.45 for Pb.
2.1. Study site 2.4. Statistical analysis The survey was conducted between June 1999 and October 2000 in the Notecka Forest (lowlands of westcentral Poland). The Notecka Forest is the second largest forested area in Poland (1350 sq. km), 100 km long and 20 km in width, nestled between the Warta and Notec´ rivers (Fig. 1). The study sites are physiographically
Analysis of variance (ANOVA) for a one-way randomized factor design was used to test whether or not mushroom species or part of the fruiting body (cap or stipe) influenced element concentrations of tested fungi. The statistical software package, Statistica 5.1, was used.
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Fig. 1. Location of the sampling area.
3. Results and discussion The ranges of macro- and microelement concentrations in the topsoil of sites where fruiting bodies were sampled are presented in Table 1. The pHsalt of the soil in the Notecka Forest is acidic (3.15–4.03). Macroelement contents, especially N, P and K, were very low and characteristic for the poor sandy soils of the lowlands where the Notecka Forest is situated (Uggla & Uggla, 1979). Low levels of toxic metals indicate that this region is free of direct environmental pollution. Only aluminium content was approximately two times higher than more neutral soils in other studies (Reich, Oleksyn, & Tjoelker, 1994; Rudawska, KieliszewskaRokicka, Leski, & Oleksyn, 1995) and was closely connected with soil acidity. The amounts of other extractable metals were also very low and did not reach the levels considered ‘‘normal’’ for the light, sandy soils in Poland (Mn: 80–710 mg kg 1; Zn: 10–200 mg kg 1, Table 1 pH and macro- and micro-element contents in the soil from the Notecka Forest in west-central Poland (g kg 1 and mg kg 1, respectively) Soil properties pH H2O pHKCl
3.56–4.20 3.15–4.03
Macroelements (g kg 1) N P K Ca Mg S
0.3–0.6 0.2–0.4 0.6–1.0 0.7–1.2 0.1–0.3 0.07–0.15
Microelements (mg kg 1) Al Mn Fe Zn Cd Pb
91–119 16.7–21.2 47.5–65.3 1.32–1.98 0.05–0.10 2.1–3.6
Cd: 0.08–1.6 mg kg 1, Pb: 5–25 mg kg 1; Kabata-Pendias & Pendias, 1999). The mean concentrations for each analyzed macroelement in the whole fruiting body, together with details for each individual species in cap and stipes, are shown in Table 2. The highest mean of concentration, on a dry mass basis, was found for N (40.5 g kg 1), followed by K (32.8 g kg 1), P (5.3 g kg 1), S (2.2 g kg 1), Ca (1.0 g kg 1), and Mg (0.7 g kg 1). There was a consistent pattern of increased levels of N accumulation occurring in conjunction with elevated P levels in the fruiting bodies of some species. Xerocomus chrysenteron, Amanita rubescens, and X. badius had the highest concentrations of N (68.7, 52.1, and 49.5 g kg 1, respectively) and fruiting bodies of these same species (A. rubescens, X. chrysenteron and X. badius) also had the highest phosphorus contents (8.2, 7.7, and 5.7 g kg 1, respectively). The lowest contents of N and P were found in Leccinum scabrum (22.1 and 1.4 g kg 1, respectively). The fruiting bodies of the tested mushrooms were rich in K (mean 32.8 g kg 1). The highest K concentration was measured in A. rubescens (49.3 g kg 1). Lactarius deliciosus and L. scabrum had average K contents that were slightly lower than the material as a whole. A low concentration of Ca (mean 1.0 g kg 1) was a common feature of all tested fruiting bodies. Comparatively high Ca concentrations (3.6 g kg 1) were measured in L. deliciosus. A low (mean 0.7 g kg 1) and remarkably constant level was noted in Mg. Sulfur concentration varied significantly among fungal species and ranged from 0.9 in A. rubescens to 4.4 g kg 1 in X. chrysenteron. As revealed by ANOVA analysis, in the fruiting bodies of the tested ectomycorrhizal fungi, only the contents of N and S are species-dependent and the concentrations of P, K, Ca, and Mg did not differ significantly among these species. The range of macroelement concentrations in the fruiting bodies of mushrooms from our study concurs with literature values for wild and cultivated fungi, irrespective of their geographical origin or how the fungi
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Table 2 Macronutrient concentrations (g kg 1 d.w.) in the fruiting bodies (F – whole fruiting body, C – cap, S – stipe) of eight fungal species from the Notecka Forest in west-central Poland Macronutrients (g kg 1)
Species
Amanita rubescens
Lactarius deliciosus
Lactarius rufus
Leccinum scabrum
Paxillus involutus
Suillus luteus
Xerocomus badius
Xerocomus chrysenteron
Mean
p > Fa Species Part of fruiting body
N
P
K
Ca
Mg
S
F C S F C S F C S F C S F C S F C S F C S F C S
52.1 ± 18.2 58.1 ± 12.5 45.3 ± 15.4 42.4 ± 11.1 45.5 ± 10.2 38.3 ± 10.2 29.4 ± 9.0 36.0 ± 12.1 23.8 ± 10.1 22.1 ± 6.3 17.1 ± 5.5 27.1 ± 8.4 28.5 ± 9.3 32.0 ± 10.6 25.0 ± 12.5 31.2 ± 8.1 35.3 ± 9.3 27.1 ± 5.2 49.5 ± 9.5 55.0 ± 9.1 44.0 ± 9.9 68.7 ± 14.1 73.1 ± 11.5 64.4 ± 15.2
8.2 ± 2.1 10.5 ± 3.5 5.9 ± 2.1 4.4 ± 1.1 6.6 ± 1.1 2.3 ± 0.6 4.2 ± 1.2 5.1 ± 1.0 3.3 ± 1.3 1.4 ± 0.6 1.2 ± 0.4 1.6 ± 0.6 4.9 ± 1.0 7.9 ± 2.1 2.0 ± 0.7 6.1 ± 1.4 7.6 ± 1.9 4.5 ± 0.5 5.7 ± 0.9 6.6 ± 0.9 4.7 ± 1.5 7.7 ± 1.2 8.8 ± 1.6 6.7 ± 1.1
49.3 ± 4.0 55.1 ± 5.5 43.5 ± 4.6 21.2 ± 0.9 29.3 ± 1.6 12.1 ± 0.6 29.4 ± 10.0 31.2 ± 11.2 28.6 ± 10.4 21.3 ± 11.2 10.3 ± 9.2 31.3 ± 12.4 41.4 ± 6.3 43.8 ± 8.5 39.0 ± 7.2 29.7 ± 2.1 34.1 ± 0.6 25.3 ± 4.5 34.9 ± 2.,9 36.5 ± 4.6 33.3 ± 2.8 35.6 ± 0.3 38.9 ± 0.6 32.2 ± 0.9
0.6 ± 0.2 0.4 ± 0.1 0.7 ± 0.3 3.6 ± 0.6 1.9 ± 0.5 5.3 ± 0.6. 0.6 ± 0.2 0.4 ± 0.1 0.8 ± 0.3 0.9 ± 0.2 0.8 ± 0.1 1.0 ± 0.6 0.9 ± 0.1 1.2 ± 0.3 0.6 ± 0.2 0.7 ± 0.1 0.5 ± 0.2 0.8 ± 0.1 0.7 ± 0.2 0.6 ± 0.2 0.9 ± 0.2 0.3 ± 0.1 0.2 ± 0.1 0.4 ± 0.1
0.8 ± 0.2 1.1 ± 0.5 0.6 ± 0.1 0.8 ± 0.3 1.1 ± 0.5 0.6 ± 0.1 0.6 ± 0.1 0.8 ± 0.4 0.4 ± 0.1 0.4 ± 0.1 0.3 ± 0.1 0.4 ± 0.1 0.9 ± 0.3 1.1 ± 0.4 0.7 ± 0.3 0.8 ± 0.2 1.1 ± 0.1 0.6 ± 0.2 0.9 ± 0.2 1.2 ± 0.3 0.7 ± 0.1 0.7 ± 0.1 0.9 ± 0.1 0.6 ± 0.1
0.9 ± 0.1 0.8 ± 0.1 0.9 ± 0.1 2.0 ± 0.4 2.0 ± 0.5 1.9 ± 0.5 1.5 ± 0.6 1.9 ± 0.6 1.0 ± 0.5 1.5 ± 0.3 1.4 ± 0.1 1.6 ± 0.3 2.0 ± 0.5 1.9 ± 0.7 0.2 ± 0.1 2.1 ± 0.6 2.7 ± 0.8 1.6 ± 0.5 3.4 ± 0.9 3.7 ± 0.9 3.1 ± 0.5 4.4 ± 0.8 4.5 ± 0.5 4.2 ± 0.6
F C S
40.5 ± 15.6 44.0 ± 17.6 36.8 ± 14.1
5.3 ± 2.1 6.8 ± 2.8 3.9 ± 1.9
32.8 ± 9.6 34.9 ± 12.8 30.7 ± 9.4
1.0 ± 1.1 0.75 ± 0.5 1.3 ± 1.6
0.7 ± 0.2 0.95 ± 0.3 0.58 ± 01
2.2 ± 1.1 2.4 ± 1.2 2.0 ± 1.1
** *
ns **
ns ns
ns ns
ns **
*** ns
ns, not significant; p > 0.05. *, **, and *** indicate p < 0.05, 0.01 and 0.001, respectively. a Based on ANOVA of species or part of fruiting body.
acquire nutrients (saprotrophs, necrotrophs or biotrophs) (Fogel, 1976; Harmon et al., 1994; Kreula et al., 1976; Longvah & Deosthale, 1998; Malinowska et al., 2004; Manzi et al., 1999; Sanmee et al., 2003; Tyler, 1980; Vogt & Edmonds, 1980). Even forest fertilization did not significantly change the nitrogen level in the fruiting bodies of L. rufus and Suillus variegatus (Ohtonen, 1986). This is in agreement with Vogt & Edmonds (1980) who found that individual species have the same nutrient levels in different forest ecosystems. A clear tendency toward higher macronutrient accumulations in caps than in stipes was also found. However, differences were statistically significant only for N, K, and Mg. Calcium seems to be preferably accumulated in stipes rather than in caps (Table 2). Similar trends were found in fruiting bodies of X. badius by Malinowska et al. (2004). All macroelements (N, P, K, Ca, Mg and S) were accumulated in much higher concentrations in fruiting
bodies of the tested mushrooms than were present in the forest soil where samples of fruiting bodies were collected (Tables 1 and 2). Nitrogen, P, and K concentrations (to a lesser extent Ca, Mg, and S) were also higher in fruiting bodies than in the foliage of Pinus sylvestris (Oleksyn, Reich, Karolewski, Tjoelker, & Chalupka, 1999; Oleksyn, Reich, Zytkowiak, Karolewski, & Tjoelker, 2002), an ectomycorrhizal host plant of most analyzed mushrooms. This implies that fungi have a specialized mechanism to accumulate nutrients in their fruiting bodies. Fruiting bodies were especially effective in nitrogen and potassium accumulation, despite a very low content of these elements in the soil substrate (Table 1). Extramatrical mycelia of ECM mushrooms play a key role in the uptake of nutrients from soil, proliferating in nutrient-rich sites and presumably competing effectively with other soil microorganisms (Smith & Read, 1997). ECM mycelia absorb, not only inorganic nutrients, but also mobilize organic
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Table 3 Macronutrient concentrations (mg kg 1 d.w.) in the fruiting bodies (F – whole fruiting body, C – cap, S – stipe) of eight fungal species from the Notecka Forest in west-central Poland Micronutrients (mg kg 1)
Species
Amanita rubescens
Lactarius deliciosus
Lactarius rufus
Leccinum scabrum
Paxillus involutus
Suillus luteus
Xerocomus badius
Xerocomus chrysenteron
Mean
p > Fa Species Part of fruit body
Al
Mn
Fe
Zn
Cd
Pb
F C S F C S F C S F C S F C S F C S F C S F C S
293 ± 73.3 75.0 ± 21.2 512 ± 95.1 199 ± 53.2 312 ± 112 85.0 ± 25.2 118 ± 22.1 125 ± 25.2 111 ± 38.2 365 ± 62.5 368 ± 58.9 332 ± 67.2 43.4 ± 6.3 66.3 ± 10.1 20.5 ± 4.2 8.5 ± 1.2 12.0 ± 2.4. 5.0 ± 1.1. 129 ± 26.7 198 ± 59.4 59.7 ± 15.2 243 ± 32.6 8.5 ± 3.2 476 ± 112
30.5 ± 4.5 29.7 ± 12.1 31.2 ± 2.4 18.3 ± 3.2 17.5 ± 1.2 19.2 ± 4.1 31.7 ± 9.8 28.2 ± 5.2 35.1 ± 7.5 9.9 ± 2.5 8.2 ± 1.2 11.7 ± 2.5 17.1 ± 3.5 9.9 ± 1.2 24.4 ± 5.8 13.4 ± 2.3 10.7 ± 4.2 16.1 ± 1.6 14.6 ± 1.6 14.4 ± 1.2 14.9 ± 3.2 21.9 ± 4.5 17.1 ± 3.2 26.8 ± 11.1
65.4 ± 15.6 69.7 ± 11.5 61.2 ± 15.4 28.7 ± 7.3 33.2 ± 2.5 24.3 ± 9.2 130 ± 36.5 142 ± 36.9 118 ± 34.2 16.3 ± 3.3 7.5 ± 2.1 25.2 ± 6.2 57.6 ± 16.5 70.5 ± 15.2 44.8 ± 11.2 38.3 ± 6.3 42.8 ± 6.3 33.8 ± 4.5 85.6 ± 14.1 122 ± 12.2 48.9 ± 5.6 53.6 ± 10.3 59.7 ± 10.0 47.5 ± 12.2
165 ± 19.6 176 ± 26.2 154 ± 31.1 179 ± 21.3 213 ± 25.2 146 ± 20.9 73.6 ± 18.7 83.5 ± 15.8 63.8 ± 14.5 28.6 ± 3.5 21.5 ± 1.6 35.7 ± 5.2 134 ± 21.2 128 ± 20.5 139 ± 25.2 52.7 ± 10.1 73.1 ± 21.2 32.3 ± 9.6 147 ± 30.1 157 ± 11.2 136 ± 32.2 128 ± 23.5 164 ± 25.5 91.6 ± 19.4
2.8 ± 0.6 3.3 ± 0.3 2.4 ± 0.5 1.7 ± 0.3 1.3 ± 0.1 2.1 ± 0.3 1.1 ± 0.3 1.0 ± 0.2 1.2 ± 0.2 0.89 ± 0.3 0.85 ± 0.1 0.92 ± 0.4 0.88 ± 0.2 0.83 ± 0.2 0.93 ± 0.2 1.1 ± 0.4 0.78 ± 0.5 1.4 ± 0.4 1.9 ± 1.6 2.3 ± 1.7 1.5 ± 1.7 2.9 ± 1.0 5.1 ± 1.5 0.72 ± 0.2
0.10 ± 0.03 0.10 ± 0.02 0.10 ± 0.05 5.2 ± 1.6 0.85 ± 0.5 9.5 ± 1.9 8.1 ± 2.4 6.7 ± 1.6 9.5 ± 2.5 0.10 ± 0.02 0.10 ± 0.02 0.10 ± 0.02 5.3 ± 1.6 4.1 ± 1.1 6.4 ± 1.6 1.4 ± 2.2 1.1 ± 0.8 1.6 ± 4.2 5.4 ± 5.2 6.1 ± 3.5 4.6 ± 7.2 3.2 ± 1.2 3.9 ± 3.1 2.4 ± 1.2
F C S
175 ± 123 146 ± 135 200 ± 208
19.8 ± 7.9 16.9 ± 8.1 22.4 ± 8.3
59.5 ± 35.9 68.5 ± 44.7 50.5 ± 30.1
113 ± 55.0 127 ± 63.1 99.8 ± 50.6
1.6 ± 0.8 1.9 ± 1.5 1.4 ± 0.6
3.6 ± 2.9 2.9 ± 2.8 4.3 ± 3.8
ns ns
ns ns
* ns
* ns
ns ns
ns ns
ns, not significant; p > 0.05. *, Indicates p < 0.05. a Based on ANOVA of species or part of fruiting body.
sources of N and P (Abuzinadah & Read, 1986, 1989a, 1989b; Perez-Moreno & Read, 2000). This temporary concentration of biologically important elements in fruiting bodies may play an important role in decomposition of organic matter and concomitant nutrient cycling in forest ecosystems (Gadd, 1993). The mean concentrations of microelements in the entire fruiting body, together with details for caps and stipes of each individual species, are shown in Table 3.The mean microelement concentrations, across all tested fungi, were in order: Al > Zn > Fe > Mn > Pb > Cd. There was a 34-fold difference in Al concentration between A. rubescens and S. luteus. Though in the individual species the concentrations of Al and Mn varied to some extent, statistical analysis did not reveal significant interspecific differences (Table 3). The Zn and Fe concentrations are species–specific (p < 0.05). Zn concentration ranged from 28.6 in L. scabrum to 179 mg kg 1 in L. deliciosus. An 8-fold difference in Fe concentration was found between L. rufus
and L. scabrum. Cadmium and Pb contents in the tested mushrooms were comparatively low (mean: 1.6 and 3.6 mg kg 1 for Cd and Pb, respectively). The highest Cd level was 2.9 mg kg 1 for X. chrysenteron and the lowest level was 0.88 mg kg 1 for P. involutus. Cadmium was preferably taken up by fungal fruiting bodies, irrespective of the low concentration in the soil (Table 1). The ability to accumulate Cd is a characteristic of mushrooms (Aruguete, Aldstadt, & Mueller, 1998; Gast, Jansen, Bierling, & Haanstra, 1988; Malinowska et al., 2004; Ru¨hling & So¨derstro¨m, 1990; Tyler, 1980) and is closely correlated with the presence of a binding compound, which is a genetically coded feature (Schmitt & Meisch, 1985; Vetter, 1993). Interspecies differences were not significant for Cd and Pb. There were no significant differences between cap and stipe for any microelement content (p > 0.05). The chemistry of metal interactions with the soil matrix is central to the uptake of metals by ECM mycelia and further accumulation in ECM fruiting bodies. In
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general, sorption to soil particles reduces the activity of metals in the system. Thus, the higher the cation-exchange capacity of the soil, the greater are the sorption and immobilization of metals (Babich & Stotzky, 1980; Gadd & Griffiths, 1978). In acidic soils, as in the Notecka Forest, metal desorption from soil binding sites into solution is enhanced due to H+ competition for binding sites, and appears to be metal specific. Aluminium, Zn, and Cd uptakes in the fruiting bodies of the tested mushrooms were notably influenced by soil acidity, but the remaining metals (Mn, Fe and Pb) showed small pHdependence. The occurrence and distribution of different macroand microelements in fruiting bodies of certain mushrooms is not only an important problem for physiology and ecology of fungi, but also has practical environmental and toxicological aspects. As evident in this and several other studies (Aruguete et al., 1998; Demirbasß, 2000; Falandysz et al., 2002; Malinowska et al., 2004; Ru¨hling & So¨derstro¨m, 1990), the mycelia of ECM fungi preferably takeup and further accumulate several highly toxic substances (in fruiting bodies), irrespective of the soil concentration. This may be important in areas where mushroom harvesting is a common practice. Poles have long taken an active interest in harvesting edible wild mushrooms from the forest, enjoying the flavour of bolets, chanterelles and other. Some species are particularly popular and are exported to European destinations (e.g. Boletus edulis, Cantharellus cibarius, X.
badius) (Statistical Yearbook – Forestry, 2003). Some other edible species are harvested in minor amounts or are collected only for domestic use, because they are not very suitable for long-distance transport (L. scabrum, L. deliciosus, S. luteus). As harvesting of mushrooms in forests, either commercially or recreationally, is increasing, it is important to ensure that mushroom resource is safe and that toxic element contents are kept within limits safe for human health. All mushroom species analyzed in this paper may be considered as edible. However, the edibility of some of them is problematic. A. rubescens and L. rufus are edible if cooked, but could cause poisoning when eaten raw. Moreover, L. rufus has been classified as an inedible mushroom due to its stinging taste. P. involutus is a popular species in some parts of Europe. Some people can eat this widespread mushroom without adverse effects. However, it frequently causes gastric distress and occasionally causes fatal hemolytic symptoms. The literature reports that, although initial consumption is fine, repeated ingestion can be fatal, as toxins from the mushroom build up in the body. Currently this species is considered poisonous and is not collected in Poland. L. deliciosus is a highly appreciated edible mushroom, but very rare and thus unimportant in terms of toxicity. X. chrysenteron is not very abundant, and is a rarely collected edible mushroom. Fruiting bodies of S. luteus, and especially X. badius, are commonly collected during the harvest season in Poland. During the past 20–30
7
25 (a)
(b)
6 20
Pb (mg kg-1 d.w.)
Cd (mg kg-1 d.w.)
5
4
3
15
10
2 5 1
0
0 1
2
3
4
5
6
7
8
9
10
1
2
sample
cap
3
4
5
6
7
8
9
10
sample
stipe
Polish statutory limit
EC statutory limit
Fig. 2. Cadmium (a) and lead (b) contents in caps and stipes of individual samples (n = 10) of X. badius collected in different places in the Notecka Forest in west-central Poland. Horizontal lines indicate: Polish (solid line) and European (dashed line) statutory limits for Cd and Pb concentrations in dried mushrooms.
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years, significant declines in the availability of certain mushrooms (chanterelles and bolets) in Poland have been observed. At the same time, the crop of X. badius increased 4-fold; 408 and 969 tons of X. badius was purchased in the years 2001 and 2002, respectively, and nearly half of them originated from the Notecka Forest (Statistical Yearbook – Forestry, 2003). Certain countries have established statutory limits for metals in edible mushrooms. In the Czech Republic, limits of 2.0 and 10.0 mg kg 1 dry matter have been established for Cd and Pb, respectively, in wild-growing mushrooms; whereas 1.0 and 10 mg kg 1 dry matter have been established for cultivated mushrooms (Kalacˇ & Svoboda, 2000). In Poland, recommendations concerning the concentrations of Cd and Pb in dried mushrooms are slightly different. The tolerance limits set for Cd and Pb are 1.0 and 2.0 mg kg 1 dry weight, respectively (Dziennik Ustaw, No. 9, position 72, 2001). The maximum level for certain contaminants in foodstuffs established by the Commission of the European Communities (Commission Regulation [EC] No 466/ 2001) is set at about 0.2 and 0.3 mg kg 1 wet weight for Cd and Pb, respectively, in cultivated fungi. Assuming that the dry matter content of mushrooms is 10% (Kalacˇ & Svoboda, 2000), these same limits for dry material will be ten times higher and approach 2.0 and 3.0 mg kg 1 dry weight for Cd and Pb, respectively. In Fig. 2(a) and (b) the range of Cd and Pb contents in caps and stipes of individual samples (n = 10) of X. badius collected in different places in the Notecka Forest are shown in relation to the statutory limits of Poland and the European Community. The results showed that most samples of X. badius from the Notecka Forest had elevated Pb concentrations (mean: 5.4 mg kg 1) and exceeded both the Polish and European tolerance limits set for dried mushrooms (Fig. 2(b)). The cadmium content in most fruiting bodies of X. badius was higher than the Polish limits, but below European statutory limits (Fig. 2(a)). The significance to human health of the element concentrations found in fruiting bodies of edible fungi may also be assessed by comparing estimated exposures with exposures from a normal diet and with the internationally agreed exposure guidelines, where these exist. These guidelines are the Provisional Tolerable Weekly Intakes (PTWIs) or Provisional Maximum Tolerable Daily Intakes (PMTDIs) set by the Joint Expert Committee on Food Additives (JECFA) of the Food and Agriculture Organization of the United Nations and the World Health Organization (FAO/WHO, 1989). Acceptable weekly intakes of Cd and Pb for adults are 0.42–0.49 and 1.5–1.75 mg, respectively. For calculations, usually 300 g of fresh mushrooms per meal is assumed (Kalacˇ & Svoboda, 2000). In relation to FAO/WHO guidelines, the PTWI for Cd is exceeded in the case of X. chrysenteron
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(2.1-fold), A. rubescens (2.0-fold), and X. badius (1.4-fold) and for lead only in case of L. rufus (1.6-fold). Consumption of mushrooms during the harvest season is very often much higher than 300 g of fresh weight/person/week. The estimated dietary exposures to Pb and Cd by consumers of mushrooms from the Notecka Forest may exceed the appropriate guidelines on safe exposures and, therefore, mushrooms should be consumed with caution.
Acknowledgements We appreciate the technical assistance of Halina Narozna and Malgorzata Luczak. We also thank Dr. Mark Tjoelker for thoughtful reading of the manuscript and English correction. The authors also appreciate the critical comments made by the referee.
References Abuzinadah, R. A., & Read, D. J. (1986). The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. I. Utilization of peptides and proteins by ectomycorrhizal fungi. New Phytologist, 103, 481–493. Abuzinadah, R. A., & Read, D. J. (1989a). The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. IV. The utilization of peptides by birch (Betula pendula L.) infected with different mycorrhizal fungi. New Phytologist, 112, 55–60. Abuzinadah, R. A., & Read, D. J. (1989b). The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. V. Nitrogen transfer in birch (Betula pendula) grown in association with mycorrhizal and non-mycorrhizal fungi. New Phytologist, 112, 61–68. Aletor, V. A. (1985). Compositional studies on edible tropical species of mushrooms. Food Chemistry, 54, 265–268. Alofe, F. V., Odeyemi, O., & Oke, O. L. (1996). Three edible wild mushroom from Nigeria: Their proximate and mineral composition. Plant Foods for Human Nutrition, 49, 63–73. Alonso, J., Garcia, M. A., Pe´rez-Lo´pez, M., & Melgar, M. J. (2003). The concentration and bioconcentration factors of copper and zinc in edible mushrooms. Archives of Environmental Contamination and Toxicology, 44, 180–188. Aruguete, D. M., Aldstadt, J. H., & Mueller, G. M. (1998). Accumulation of several heavy metals and lanthanides in mushrooms (Agaricales) from the Chicago region. The Science of the Total Environment, 224, 43–56. Babich, H., & Stotzky, G. (1980). Environmental factors that influence the toxicity of heavy metal and gaseous pollutants to micoorganisms. Critical Reviews of Microbiology, 8, 99–145. Commission Regulation (EC) No 466/2001 of 8 March 2001 setting maximum levels of certain contaminants in foodstuffs. Official Journal of the European Communities, 16.3.2001. L77/1-13. Demirbasß, A. (2000). Accumulation of heavy metals in some edible mushrooms from Turkey. Food Chemistry, 68, 415–419. Dı´ez, V. A., & Alvarez, A. (2001). Compositional and nutritional studies on two wild edible mushrooms from northwest Spain. Food Chemistry, 75, 417–422. Dziennik Ustaw, No 9, position 72, Warsaw, Poland, 2001. FAO/WHO. (1989). Evaluation of certain food additives and contaminants, 33. Report of the Joint FAO/WHO. WHO Technical Report Series 776.
506
M. Rudawska, T. Leski / Food Chemistry 92 (2005) 499–506
Falandysz, J., Danisiewicz, D., & Bona, H. (1994). Metals content of wild growing mushrooms gathered in the Tucholskie and Kaszuby Forests. Bromatologia i Chemia Toksylogiczna, 2, 135–139. Falandysz, J., Szymczyk, K., Ichihashi, H., Bielawski, L., Gucia, M., Frankowska, A., et al. (2001). ICP/MS and ICP/AES elemental analysis (38 elements) of edible wild mushrooms growing in Poland. Food Additives and Contaminants, 6, 503–513. Falandysz, J., Lipka, K., Gucia, M., Kawano, M., Strumnik, K., & Kannan, K. (2002). Accumulation factors of mercury in mushrooms from Zaborski Landscape Park, Poland. Environment International, 28, 421–427. Fogel, R. (1976). Ecological studies of hypogeous fungi. II. Sporocarp phenology in a western Oregon Douglas Fir stand. Canadian Journal of Botany, 54, 1152–1162. Gadd, G. M. (1993). Interactions of fungi with toxic metals. New Phytologist, 124, 25–60. Gadd, G. M., & Griffiths, A. J. (1978). Microorganisms and heavy metal toxicity. Microbial Ecology, 4, 303–317. Gast, C. H., Jansen, E., Bierling, J., & Haanstra, L. (1988). Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere, 17, 789–799. Grzybek, J., & Janczy, B. (1990). Quantitative estimation of lead, cadmium, and nickel content by means of Atomic Absorption Spectroscopy in fruit bodies of some macromycetes in Poland. Acta Mycologica, 26, 17–23. Harmon, M. E., Sexton, J., Caldwell, B. A., & Carpenter, S. E. (1994). Fungal sporocarp mediated losses of Ca, Fe, K, Mg, Mn, N, P and Zn from conifer logs in the early stages of decomposition. Canadian Journal of Forerest Research, 24, 1883–1893. Kabata-Pendias, A., & Pendias, H. (1999). Biogeochemistry of trace elements. Warsaw: PWN. Kalacˇ, P., & Svoboda, L. A. (2000). Review of trace element concentrations in edible mushrooms. Food Chemistry, 62, 273–281. Kreula, M., Saarivirta, M., & Karanko, S.-L. (1976). On the composition of nutrients in wild and cultivated mushrooms. Karstenia, 16, 10–14. Latiff, L. A., Daran, A. B. M., & Mohamed, A. B. (1996). Relative distribution of minerals in the pileus and stalk of some selected edible mushrooms. Food Chemistry, 56, 115–121. Longvah, T., & Deosthale, Y. G. (1998). Compositional and nutritional studies on edible wild mushroom from northeast India. Food Chemistry, 63, 331–334. Malinowska, E., Szafer, P., & Falandysz, J. (2004). Metals bioaccumulation by bay bolete, Xerocomus badius, from selected sites in Poland. Food Chemistry, 84, 405–416. Manzi, P., Aguzzi, A., & Pizzoferrato, L. (2001). Nutritional value of mushrooms widely consumed in Italy. Food Chemistry, 73, 321–325. Manzi, P., Gambelli, L., Marconi, S., Vivanti, V., & Pizzoferrato, L. (1999). Nutrients in edible mushrooms: an inter-species comparative study. Food Chemistry, 65, 477–482. Ohtonen, R. (1986). The effect of forest fertilization on the nitrogen content of the fruit-bodies of two mycorrhizal fungi, Lactarius
rufus and Suillus variegatus. Annales Botanici Fennici, 23, 189–203. Oleksyn, J., Reich, P. B., Karolewski, P., Tjoelker, M. G., & Chalupka, W. (1999). Nutritional status of pollen and needles of diverse Pinus sylvestris populations grown at sites with contrasting pollution. Water Air and Soil Pollution, 110, 195–212. Oleksyn, J., Reich, P. B., Zytkowiak, R., Karolewski, P., & Tjoelker, M. G. (2002). Needle nutrients in geographically diverse Pinus sylvestris L. populations. Annals of Forest Science, 59, 1–18. Perez-Moreno, J., & Read, D. J. (2000). Mobilization and transfer of nutrients from litter to tree seedlings via the vegetative mycelium of ectomycorrhizal plants. New Phytologist, 145, 301–309. Reich, P. B., Oleksyn, J., & Tjoelker, M. G. (1994). Relationship of aluminium and calcium to net CO2 exchange among diverse Scots pine provenances under pollution stress in Polanad. Oecologia, 97, 82–92. Rudawska, M., Kieliszewska-Rokicka, B., Leski, T., & Oleksyn, J. (1995). Mycorrhizal status of a Scots pine (Pinus sylvestris L.) plantation affected by pollution from a phosphate fertilizer plant. Water Air and Soil Pollution, 85, 1281–1286. Ru¨hling, A., & So¨derstro¨m, B. (1990). Changes in fruitbodies production of mycorrhizal and litter decomposing macromycetes in heavy metal polluted coniferous forest in North Sweden. Water Air and Soil Pollution, 49, 375–387. Sanmee, R., Dell, B., Lumyong, P., Izumori, K., & Lumyong, S. (2003). Nutritive value of popular wild edible mushrooms from northern Thailand. Food Chemistry, 82, 527–532. Senatore, F., Dini, A., & Marino, A. (1988). Chemical constituents of some basidiomycetes. Journal of Science of Food and Agriculture, 45, 337–345. Schmitt, J. A., & Meisch, H. U. (1985). Cadmium in mushrooms, distribution growth effects and binding. Trace Elements in Medicine, 2, 163–166. Smith, S. E., & Read, D. J. (1997). Mycorrhizal symbiosis (2nd ed.). Academic Press. Statistical Yearbook – Forestry. (2003). Warsaw: Central Statistical Office. Tshinyangu, K. K. (1996). Effect of grass hay substrate on nutritional value of Pleurotus ostreatus var. colombinus. Die Nahrung, 40, 79–83. Turnau, K. (1991). The influence of cadmium dust on fungi in a PinoQuercetum forest. Ekologia Polska, 39, 39–57. Tyler, G. (1980). Metals in sporophores of basidiomycetes. Transactions of the British Mycological Society, 74, 41–49. Uggla, H., & Uggla, Z. (1979). Forest pedology (in polish). Warsaw: PWRiL. Vetter, J. (1993). Toxic elements in certain higher fungi. Food Chemistry, 48, 207–208. Vogt, K. A., & Edmonds, R. L. (1980). Patterns of nutrient concentration in basidiocarps in western Washington. Canadian Journal of Botany, 58, 694–698.
Macro- and microelement contents in fruiting bodies of wild mushrooms from the Notecka forest in west-central Poland Maria Rudawska *, Tomasz Leski Institute of Dendrology, Polish Academy of Sciences, 5 Parkowa Str., 62-035 Ko´rnik, Poland Received 26 April 2004; received in revised form 17 August 2004; accepted 17 August 2004
Abstract Fruiting bodies of wild mushrooms and forest soil samples were collected and analyzed for macro- (N, P, K, S, Ca, Mg) and microelement (Al, Zn, Fe, Mn, Cd, Pb) contents in pine stands of the Notecka Forest in west-central Poland. Elements were determined by atomic absorption spectrometry in 160 samples of 8 fungal species and 15 underlying soil samples. Macro- and microelement contents in soil were low and characteristic of the poor and acidic sandy soils of the Polish lowlands not influenced by industrial pollution. In fruiting bodies, the highest mean concentration of macroelements (dry mass basis) was found for N (40.0 g kg 1), followed by K (33.0 g kg 1), P (5.4 g kg 1), S (2.2 g kg 1), Ca (1.0 g kg 1) and Mg (0.7 g kg 1). All macroelements (except for Ca) were concentrated in considerably higher levels in the fruiting bodies than in the forest soil. Nitrogen, P, K, S and Mg were preferably translocated into the cap rather than the stipes. Calcium, however, was often found in higher concentration in stipes than in caps. The mean microelement concentrations, across all tested fungi, were in the following order: Al > Zn > Fe > Mn > Pb > Cd. Microelements showed different distributions, depending on the part of the fruiting body. Some were more concentrated in the caps and some in stipes and distributions varied among species. Xerocomus badius is the most often harvested edible mushroom in the Notecka Forest. Pb and Cd distributions in fruiting bodies of this mushroom were evaluated in order to assess health risks to consumers. The estimated dietary exposures to Pb and Cd for consumers of this mushroom were in excess of guidelines on safe exposures. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Essential elements; Trace metals; Ectomycorrhizal fungi; Edible mushrooms
1. Introduction Fungi are important organisms in nature and are present almost everywhere. There are numerous species of wild mushrooms and many are edible. Mushrooms do not constitute a significant portion of the human diet; however, the consumption of wild and cultivated mushrooms continues to increase in many countries (e.g., Alonso, Garcia, Pe´rez-Lo´pez, & Melgar, 2003; Demirbasß, 2000; Falandysz et al., 2001; Kalacˇ & Svoboda, 2000; Latiff, Daran, & Mohamed, 1996; Longvah & *
Corresponding author. Tel.: +48 61 8170033/8170166; fax: +48 61 8170166. E-mail address: [email protected] (M. Rudawska). 0308-8146/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodchem.2004.08.017
Deosthale, 1998; Manzi, Aguzzi, & Pizzoferrato, 2001; Sanmee, Dell, Lumyong, Izumori, & Lumyong, 2003). Many common mushrooms, for example, Amanita, Suillus, Xerocomus, Lactarius, Russula, Leccinum and Paxillus, are ectomycorrhizal (ECM). External mycelia of ECM fungi (vegetative phase) spread below-ground around trees, acquiring water and minerals from the soil to benefit trees in symbiotic associations (Smith & Read, 1997). Fungal fruiting bodies are also connected to host roots through mycelia which transport carbohydrates necessary for their development. During rainy seasons, the fruiting bodies of ECM fungi can be seen in forests. They represent a visible by-product of ECM mycelia and function as reproductive structures. The chemical composition and nutritional quality of different wild
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and cultivated mushroom species have been studied (Aletor, 1985; Alofe, Odeyemi, & Oke, 1996; Dı´ez & Alvarez, 2001; Kreula, Saarivirta, & Karanko, 1976; Longvah & Deosthale, 1998; Manzi et al., 2001; Manzi, Gambelli, Marconi, Vivanti, & Pizzoferrato, 1999; Senatore, Dini, & Marino, 1988; Tshinyangu, 1996). Besides water (85–95% f.w.), carbohydrates (39.9% d.w.), proteins (17.5% d.w.) and low contents of lipids (2.9% d.w.) (Latiff et al., 1996), the wide variety and abundance of minerals are the most characteristic features of ECM fruiting bodies. Macro- and microelements present in the environment are to different extents accumulated by ECM vegetative mycelia and in the ECM fruiting bodies (Harmon, Sexton, Caldwell, & Carpenter, 1994; Kreula et al., 1976; Sanmee et al., 2003; Vogt & Edmonds, 1980). Several studies have been carried out on the trace element contents in fruiting bodies of the wild-growing edible mushrooms in Poland. The major publications consider levels of heavy metals in groups of mushrooms comprised of various species and collected in highly polluted or control sites (Falandysz, Danisiewicz, & Bona, 1994; Grzybek & Janczy, 1990; Malinowska, Szafer, & Falandysz, 2004; Turnau, 1991). Data on the general patterns of macro- and microelement accumulations in fruiting bodies of wild, ECM fungi in Poland are scarce and limited to a few sites in the Pomorskie Voivodeship in northern Poland (Falandysz et al., 2001; Malinowska et al., 2004). Poland is the largest producer of wild mushrooms in Europe and the largest European exporter of edible mushrooms. Commercial harvesting of mushrooms in Poland has a long tradition. A total of 1.71, 3.28, and 2.38 million kg of mushrooms were purchased by the food industry in 2000, 2001 and 2002, respectively (Statistical Yearbook – Forestry, 2003). Of this total, around half (depending on the year) originated from the Notecka Forest situated in west-central Poland. This study was initiated to (1) evaluate macro- and microelement contents in fruiting bodies of wild grown, mostly edible ectomycorrhizal fungi collected in the Notecka Forest region, and (2) determine which toxic metals were accumulated in higher concentrations in fruiting bodies of a frequently harvested and eaten mushroom, X. badius, in order to assess the health risks to consumers.
2. Materials and methods
homogeneous, both with regard to landscape formation and forest vegetation. Soils of this area are influenced mostly by planting haplic podzol and inland dunes with Scots pine (Pinus sylvestris) as the dominant tree species (95%). The Notecka Forest is situated far away from the acute sources of industrial pollution and is considered to be one of the most important centres for commercial harvesting of mushrooms in Poland. 2.2. Mushrooms and soil sampling The fruiting bodies of eight mushrooms species, namely Amanita rubescens, Lactarius deliciosus, L. rufus, Leccinum scabrum, Paxillus involutus, Suillus luteus, Xerocomus badius, and X. chrysenteron, were selected for this study. All these mushrooms have been consumed; however, the edibility of P. involutus and L. rufus is problematic (see Section 3). Fruiting bodies (2–4 fruiting bodies of each species per site) collected in five different areas of the Notecka Forest were divided into the cap and stipe, rinsed in deionized water to remove adhering particles, dried at 60 °C for 48 h, and ground in an automatic mortar; 160 samples of fleshy fruiting bodies (80 caps and 80 stipes) were analyzed. In addition to the mushroom collection, 15 soil samples of the upper forest soil horizon (0–10 cm, after removing the surface layer of organic detritus) were also collected at appropriate sampling places. 2.3. Chemical analysis Soil samples and milled fruiting bodies, of approximately 2.5 g d.w. each, were digested in a mixture of spectrally pure concentrated acids: HNO3 and HClO4 in a proportion of 4:1 (v:v) and diluted with bi-distilled water to make 25 ml. Nitrogen was analyzed by the micro-Kjeldahl method. The rest of the macroelements, aluminium, and heavy metals (Mn, Fe, Zn, Cd and Pb), were measured by atomic absorption spectroscopy (Varian 220 FS) with atomization in an air-acetylene flame. The accuracy of the analyses was checked against standard reference material, namely pine needles SRM 1575 and tomato leaves SRM 1573a (National Institute of Standards and Technology). Detection limit values of microelements, in microgrammes per litre were found to be 1.3 for Al, 0.05 for Mn, 0.11 for Fe, 0.02 for Zn, 0.02 for Cd, and 0.45 for Pb.
2.1. Study site 2.4. Statistical analysis The survey was conducted between June 1999 and October 2000 in the Notecka Forest (lowlands of westcentral Poland). The Notecka Forest is the second largest forested area in Poland (1350 sq. km), 100 km long and 20 km in width, nestled between the Warta and Notec´ rivers (Fig. 1). The study sites are physiographically
Analysis of variance (ANOVA) for a one-way randomized factor design was used to test whether or not mushroom species or part of the fruiting body (cap or stipe) influenced element concentrations of tested fungi. The statistical software package, Statistica 5.1, was used.
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Fig. 1. Location of the sampling area.
3. Results and discussion The ranges of macro- and microelement concentrations in the topsoil of sites where fruiting bodies were sampled are presented in Table 1. The pHsalt of the soil in the Notecka Forest is acidic (3.15–4.03). Macroelement contents, especially N, P and K, were very low and characteristic for the poor sandy soils of the lowlands where the Notecka Forest is situated (Uggla & Uggla, 1979). Low levels of toxic metals indicate that this region is free of direct environmental pollution. Only aluminium content was approximately two times higher than more neutral soils in other studies (Reich, Oleksyn, & Tjoelker, 1994; Rudawska, KieliszewskaRokicka, Leski, & Oleksyn, 1995) and was closely connected with soil acidity. The amounts of other extractable metals were also very low and did not reach the levels considered ‘‘normal’’ for the light, sandy soils in Poland (Mn: 80–710 mg kg 1; Zn: 10–200 mg kg 1, Table 1 pH and macro- and micro-element contents in the soil from the Notecka Forest in west-central Poland (g kg 1 and mg kg 1, respectively) Soil properties pH H2O pHKCl
3.56–4.20 3.15–4.03
Macroelements (g kg 1) N P K Ca Mg S
0.3–0.6 0.2–0.4 0.6–1.0 0.7–1.2 0.1–0.3 0.07–0.15
Microelements (mg kg 1) Al Mn Fe Zn Cd Pb
91–119 16.7–21.2 47.5–65.3 1.32–1.98 0.05–0.10 2.1–3.6
Cd: 0.08–1.6 mg kg 1, Pb: 5–25 mg kg 1; Kabata-Pendias & Pendias, 1999). The mean concentrations for each analyzed macroelement in the whole fruiting body, together with details for each individual species in cap and stipes, are shown in Table 2. The highest mean of concentration, on a dry mass basis, was found for N (40.5 g kg 1), followed by K (32.8 g kg 1), P (5.3 g kg 1), S (2.2 g kg 1), Ca (1.0 g kg 1), and Mg (0.7 g kg 1). There was a consistent pattern of increased levels of N accumulation occurring in conjunction with elevated P levels in the fruiting bodies of some species. Xerocomus chrysenteron, Amanita rubescens, and X. badius had the highest concentrations of N (68.7, 52.1, and 49.5 g kg 1, respectively) and fruiting bodies of these same species (A. rubescens, X. chrysenteron and X. badius) also had the highest phosphorus contents (8.2, 7.7, and 5.7 g kg 1, respectively). The lowest contents of N and P were found in Leccinum scabrum (22.1 and 1.4 g kg 1, respectively). The fruiting bodies of the tested mushrooms were rich in K (mean 32.8 g kg 1). The highest K concentration was measured in A. rubescens (49.3 g kg 1). Lactarius deliciosus and L. scabrum had average K contents that were slightly lower than the material as a whole. A low concentration of Ca (mean 1.0 g kg 1) was a common feature of all tested fruiting bodies. Comparatively high Ca concentrations (3.6 g kg 1) were measured in L. deliciosus. A low (mean 0.7 g kg 1) and remarkably constant level was noted in Mg. Sulfur concentration varied significantly among fungal species and ranged from 0.9 in A. rubescens to 4.4 g kg 1 in X. chrysenteron. As revealed by ANOVA analysis, in the fruiting bodies of the tested ectomycorrhizal fungi, only the contents of N and S are species-dependent and the concentrations of P, K, Ca, and Mg did not differ significantly among these species. The range of macroelement concentrations in the fruiting bodies of mushrooms from our study concurs with literature values for wild and cultivated fungi, irrespective of their geographical origin or how the fungi
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Table 2 Macronutrient concentrations (g kg 1 d.w.) in the fruiting bodies (F – whole fruiting body, C – cap, S – stipe) of eight fungal species from the Notecka Forest in west-central Poland Macronutrients (g kg 1)
Species
Amanita rubescens
Lactarius deliciosus
Lactarius rufus
Leccinum scabrum
Paxillus involutus
Suillus luteus
Xerocomus badius
Xerocomus chrysenteron
Mean
p > Fa Species Part of fruiting body
N
P
K
Ca
Mg
S
F C S F C S F C S F C S F C S F C S F C S F C S
52.1 ± 18.2 58.1 ± 12.5 45.3 ± 15.4 42.4 ± 11.1 45.5 ± 10.2 38.3 ± 10.2 29.4 ± 9.0 36.0 ± 12.1 23.8 ± 10.1 22.1 ± 6.3 17.1 ± 5.5 27.1 ± 8.4 28.5 ± 9.3 32.0 ± 10.6 25.0 ± 12.5 31.2 ± 8.1 35.3 ± 9.3 27.1 ± 5.2 49.5 ± 9.5 55.0 ± 9.1 44.0 ± 9.9 68.7 ± 14.1 73.1 ± 11.5 64.4 ± 15.2
8.2 ± 2.1 10.5 ± 3.5 5.9 ± 2.1 4.4 ± 1.1 6.6 ± 1.1 2.3 ± 0.6 4.2 ± 1.2 5.1 ± 1.0 3.3 ± 1.3 1.4 ± 0.6 1.2 ± 0.4 1.6 ± 0.6 4.9 ± 1.0 7.9 ± 2.1 2.0 ± 0.7 6.1 ± 1.4 7.6 ± 1.9 4.5 ± 0.5 5.7 ± 0.9 6.6 ± 0.9 4.7 ± 1.5 7.7 ± 1.2 8.8 ± 1.6 6.7 ± 1.1
49.3 ± 4.0 55.1 ± 5.5 43.5 ± 4.6 21.2 ± 0.9 29.3 ± 1.6 12.1 ± 0.6 29.4 ± 10.0 31.2 ± 11.2 28.6 ± 10.4 21.3 ± 11.2 10.3 ± 9.2 31.3 ± 12.4 41.4 ± 6.3 43.8 ± 8.5 39.0 ± 7.2 29.7 ± 2.1 34.1 ± 0.6 25.3 ± 4.5 34.9 ± 2.,9 36.5 ± 4.6 33.3 ± 2.8 35.6 ± 0.3 38.9 ± 0.6 32.2 ± 0.9
0.6 ± 0.2 0.4 ± 0.1 0.7 ± 0.3 3.6 ± 0.6 1.9 ± 0.5 5.3 ± 0.6. 0.6 ± 0.2 0.4 ± 0.1 0.8 ± 0.3 0.9 ± 0.2 0.8 ± 0.1 1.0 ± 0.6 0.9 ± 0.1 1.2 ± 0.3 0.6 ± 0.2 0.7 ± 0.1 0.5 ± 0.2 0.8 ± 0.1 0.7 ± 0.2 0.6 ± 0.2 0.9 ± 0.2 0.3 ± 0.1 0.2 ± 0.1 0.4 ± 0.1
0.8 ± 0.2 1.1 ± 0.5 0.6 ± 0.1 0.8 ± 0.3 1.1 ± 0.5 0.6 ± 0.1 0.6 ± 0.1 0.8 ± 0.4 0.4 ± 0.1 0.4 ± 0.1 0.3 ± 0.1 0.4 ± 0.1 0.9 ± 0.3 1.1 ± 0.4 0.7 ± 0.3 0.8 ± 0.2 1.1 ± 0.1 0.6 ± 0.2 0.9 ± 0.2 1.2 ± 0.3 0.7 ± 0.1 0.7 ± 0.1 0.9 ± 0.1 0.6 ± 0.1
0.9 ± 0.1 0.8 ± 0.1 0.9 ± 0.1 2.0 ± 0.4 2.0 ± 0.5 1.9 ± 0.5 1.5 ± 0.6 1.9 ± 0.6 1.0 ± 0.5 1.5 ± 0.3 1.4 ± 0.1 1.6 ± 0.3 2.0 ± 0.5 1.9 ± 0.7 0.2 ± 0.1 2.1 ± 0.6 2.7 ± 0.8 1.6 ± 0.5 3.4 ± 0.9 3.7 ± 0.9 3.1 ± 0.5 4.4 ± 0.8 4.5 ± 0.5 4.2 ± 0.6
F C S
40.5 ± 15.6 44.0 ± 17.6 36.8 ± 14.1
5.3 ± 2.1 6.8 ± 2.8 3.9 ± 1.9
32.8 ± 9.6 34.9 ± 12.8 30.7 ± 9.4
1.0 ± 1.1 0.75 ± 0.5 1.3 ± 1.6
0.7 ± 0.2 0.95 ± 0.3 0.58 ± 01
2.2 ± 1.1 2.4 ± 1.2 2.0 ± 1.1
** *
ns **
ns ns
ns ns
ns **
*** ns
ns, not significant; p > 0.05. *, **, and *** indicate p < 0.05, 0.01 and 0.001, respectively. a Based on ANOVA of species or part of fruiting body.
acquire nutrients (saprotrophs, necrotrophs or biotrophs) (Fogel, 1976; Harmon et al., 1994; Kreula et al., 1976; Longvah & Deosthale, 1998; Malinowska et al., 2004; Manzi et al., 1999; Sanmee et al., 2003; Tyler, 1980; Vogt & Edmonds, 1980). Even forest fertilization did not significantly change the nitrogen level in the fruiting bodies of L. rufus and Suillus variegatus (Ohtonen, 1986). This is in agreement with Vogt & Edmonds (1980) who found that individual species have the same nutrient levels in different forest ecosystems. A clear tendency toward higher macronutrient accumulations in caps than in stipes was also found. However, differences were statistically significant only for N, K, and Mg. Calcium seems to be preferably accumulated in stipes rather than in caps (Table 2). Similar trends were found in fruiting bodies of X. badius by Malinowska et al. (2004). All macroelements (N, P, K, Ca, Mg and S) were accumulated in much higher concentrations in fruiting
bodies of the tested mushrooms than were present in the forest soil where samples of fruiting bodies were collected (Tables 1 and 2). Nitrogen, P, and K concentrations (to a lesser extent Ca, Mg, and S) were also higher in fruiting bodies than in the foliage of Pinus sylvestris (Oleksyn, Reich, Karolewski, Tjoelker, & Chalupka, 1999; Oleksyn, Reich, Zytkowiak, Karolewski, & Tjoelker, 2002), an ectomycorrhizal host plant of most analyzed mushrooms. This implies that fungi have a specialized mechanism to accumulate nutrients in their fruiting bodies. Fruiting bodies were especially effective in nitrogen and potassium accumulation, despite a very low content of these elements in the soil substrate (Table 1). Extramatrical mycelia of ECM mushrooms play a key role in the uptake of nutrients from soil, proliferating in nutrient-rich sites and presumably competing effectively with other soil microorganisms (Smith & Read, 1997). ECM mycelia absorb, not only inorganic nutrients, but also mobilize organic
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503
Table 3 Macronutrient concentrations (mg kg 1 d.w.) in the fruiting bodies (F – whole fruiting body, C – cap, S – stipe) of eight fungal species from the Notecka Forest in west-central Poland Micronutrients (mg kg 1)
Species
Amanita rubescens
Lactarius deliciosus
Lactarius rufus
Leccinum scabrum
Paxillus involutus
Suillus luteus
Xerocomus badius
Xerocomus chrysenteron
Mean
p > Fa Species Part of fruit body
Al
Mn
Fe
Zn
Cd
Pb
F C S F C S F C S F C S F C S F C S F C S F C S
293 ± 73.3 75.0 ± 21.2 512 ± 95.1 199 ± 53.2 312 ± 112 85.0 ± 25.2 118 ± 22.1 125 ± 25.2 111 ± 38.2 365 ± 62.5 368 ± 58.9 332 ± 67.2 43.4 ± 6.3 66.3 ± 10.1 20.5 ± 4.2 8.5 ± 1.2 12.0 ± 2.4. 5.0 ± 1.1. 129 ± 26.7 198 ± 59.4 59.7 ± 15.2 243 ± 32.6 8.5 ± 3.2 476 ± 112
30.5 ± 4.5 29.7 ± 12.1 31.2 ± 2.4 18.3 ± 3.2 17.5 ± 1.2 19.2 ± 4.1 31.7 ± 9.8 28.2 ± 5.2 35.1 ± 7.5 9.9 ± 2.5 8.2 ± 1.2 11.7 ± 2.5 17.1 ± 3.5 9.9 ± 1.2 24.4 ± 5.8 13.4 ± 2.3 10.7 ± 4.2 16.1 ± 1.6 14.6 ± 1.6 14.4 ± 1.2 14.9 ± 3.2 21.9 ± 4.5 17.1 ± 3.2 26.8 ± 11.1
65.4 ± 15.6 69.7 ± 11.5 61.2 ± 15.4 28.7 ± 7.3 33.2 ± 2.5 24.3 ± 9.2 130 ± 36.5 142 ± 36.9 118 ± 34.2 16.3 ± 3.3 7.5 ± 2.1 25.2 ± 6.2 57.6 ± 16.5 70.5 ± 15.2 44.8 ± 11.2 38.3 ± 6.3 42.8 ± 6.3 33.8 ± 4.5 85.6 ± 14.1 122 ± 12.2 48.9 ± 5.6 53.6 ± 10.3 59.7 ± 10.0 47.5 ± 12.2
165 ± 19.6 176 ± 26.2 154 ± 31.1 179 ± 21.3 213 ± 25.2 146 ± 20.9 73.6 ± 18.7 83.5 ± 15.8 63.8 ± 14.5 28.6 ± 3.5 21.5 ± 1.6 35.7 ± 5.2 134 ± 21.2 128 ± 20.5 139 ± 25.2 52.7 ± 10.1 73.1 ± 21.2 32.3 ± 9.6 147 ± 30.1 157 ± 11.2 136 ± 32.2 128 ± 23.5 164 ± 25.5 91.6 ± 19.4
2.8 ± 0.6 3.3 ± 0.3 2.4 ± 0.5 1.7 ± 0.3 1.3 ± 0.1 2.1 ± 0.3 1.1 ± 0.3 1.0 ± 0.2 1.2 ± 0.2 0.89 ± 0.3 0.85 ± 0.1 0.92 ± 0.4 0.88 ± 0.2 0.83 ± 0.2 0.93 ± 0.2 1.1 ± 0.4 0.78 ± 0.5 1.4 ± 0.4 1.9 ± 1.6 2.3 ± 1.7 1.5 ± 1.7 2.9 ± 1.0 5.1 ± 1.5 0.72 ± 0.2
0.10 ± 0.03 0.10 ± 0.02 0.10 ± 0.05 5.2 ± 1.6 0.85 ± 0.5 9.5 ± 1.9 8.1 ± 2.4 6.7 ± 1.6 9.5 ± 2.5 0.10 ± 0.02 0.10 ± 0.02 0.10 ± 0.02 5.3 ± 1.6 4.1 ± 1.1 6.4 ± 1.6 1.4 ± 2.2 1.1 ± 0.8 1.6 ± 4.2 5.4 ± 5.2 6.1 ± 3.5 4.6 ± 7.2 3.2 ± 1.2 3.9 ± 3.1 2.4 ± 1.2
F C S
175 ± 123 146 ± 135 200 ± 208
19.8 ± 7.9 16.9 ± 8.1 22.4 ± 8.3
59.5 ± 35.9 68.5 ± 44.7 50.5 ± 30.1
113 ± 55.0 127 ± 63.1 99.8 ± 50.6
1.6 ± 0.8 1.9 ± 1.5 1.4 ± 0.6
3.6 ± 2.9 2.9 ± 2.8 4.3 ± 3.8
ns ns
ns ns
* ns
* ns
ns ns
ns ns
ns, not significant; p > 0.05. *, Indicates p < 0.05. a Based on ANOVA of species or part of fruiting body.
sources of N and P (Abuzinadah & Read, 1986, 1989a, 1989b; Perez-Moreno & Read, 2000). This temporary concentration of biologically important elements in fruiting bodies may play an important role in decomposition of organic matter and concomitant nutrient cycling in forest ecosystems (Gadd, 1993). The mean concentrations of microelements in the entire fruiting body, together with details for caps and stipes of each individual species, are shown in Table 3.The mean microelement concentrations, across all tested fungi, were in order: Al > Zn > Fe > Mn > Pb > Cd. There was a 34-fold difference in Al concentration between A. rubescens and S. luteus. Though in the individual species the concentrations of Al and Mn varied to some extent, statistical analysis did not reveal significant interspecific differences (Table 3). The Zn and Fe concentrations are species–specific (p < 0.05). Zn concentration ranged from 28.6 in L. scabrum to 179 mg kg 1 in L. deliciosus. An 8-fold difference in Fe concentration was found between L. rufus
and L. scabrum. Cadmium and Pb contents in the tested mushrooms were comparatively low (mean: 1.6 and 3.6 mg kg 1 for Cd and Pb, respectively). The highest Cd level was 2.9 mg kg 1 for X. chrysenteron and the lowest level was 0.88 mg kg 1 for P. involutus. Cadmium was preferably taken up by fungal fruiting bodies, irrespective of the low concentration in the soil (Table 1). The ability to accumulate Cd is a characteristic of mushrooms (Aruguete, Aldstadt, & Mueller, 1998; Gast, Jansen, Bierling, & Haanstra, 1988; Malinowska et al., 2004; Ru¨hling & So¨derstro¨m, 1990; Tyler, 1980) and is closely correlated with the presence of a binding compound, which is a genetically coded feature (Schmitt & Meisch, 1985; Vetter, 1993). Interspecies differences were not significant for Cd and Pb. There were no significant differences between cap and stipe for any microelement content (p > 0.05). The chemistry of metal interactions with the soil matrix is central to the uptake of metals by ECM mycelia and further accumulation in ECM fruiting bodies. In
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general, sorption to soil particles reduces the activity of metals in the system. Thus, the higher the cation-exchange capacity of the soil, the greater are the sorption and immobilization of metals (Babich & Stotzky, 1980; Gadd & Griffiths, 1978). In acidic soils, as in the Notecka Forest, metal desorption from soil binding sites into solution is enhanced due to H+ competition for binding sites, and appears to be metal specific. Aluminium, Zn, and Cd uptakes in the fruiting bodies of the tested mushrooms were notably influenced by soil acidity, but the remaining metals (Mn, Fe and Pb) showed small pHdependence. The occurrence and distribution of different macroand microelements in fruiting bodies of certain mushrooms is not only an important problem for physiology and ecology of fungi, but also has practical environmental and toxicological aspects. As evident in this and several other studies (Aruguete et al., 1998; Demirbasß, 2000; Falandysz et al., 2002; Malinowska et al., 2004; Ru¨hling & So¨derstro¨m, 1990), the mycelia of ECM fungi preferably takeup and further accumulate several highly toxic substances (in fruiting bodies), irrespective of the soil concentration. This may be important in areas where mushroom harvesting is a common practice. Poles have long taken an active interest in harvesting edible wild mushrooms from the forest, enjoying the flavour of bolets, chanterelles and other. Some species are particularly popular and are exported to European destinations (e.g. Boletus edulis, Cantharellus cibarius, X.
badius) (Statistical Yearbook – Forestry, 2003). Some other edible species are harvested in minor amounts or are collected only for domestic use, because they are not very suitable for long-distance transport (L. scabrum, L. deliciosus, S. luteus). As harvesting of mushrooms in forests, either commercially or recreationally, is increasing, it is important to ensure that mushroom resource is safe and that toxic element contents are kept within limits safe for human health. All mushroom species analyzed in this paper may be considered as edible. However, the edibility of some of them is problematic. A. rubescens and L. rufus are edible if cooked, but could cause poisoning when eaten raw. Moreover, L. rufus has been classified as an inedible mushroom due to its stinging taste. P. involutus is a popular species in some parts of Europe. Some people can eat this widespread mushroom without adverse effects. However, it frequently causes gastric distress and occasionally causes fatal hemolytic symptoms. The literature reports that, although initial consumption is fine, repeated ingestion can be fatal, as toxins from the mushroom build up in the body. Currently this species is considered poisonous and is not collected in Poland. L. deliciosus is a highly appreciated edible mushroom, but very rare and thus unimportant in terms of toxicity. X. chrysenteron is not very abundant, and is a rarely collected edible mushroom. Fruiting bodies of S. luteus, and especially X. badius, are commonly collected during the harvest season in Poland. During the past 20–30
7
25 (a)
(b)
6 20
Pb (mg kg-1 d.w.)
Cd (mg kg-1 d.w.)
5
4
3
15
10
2 5 1
0
0 1
2
3
4
5
6
7
8
9
10
1
2
sample
cap
3
4
5
6
7
8
9
10
sample
stipe
Polish statutory limit
EC statutory limit
Fig. 2. Cadmium (a) and lead (b) contents in caps and stipes of individual samples (n = 10) of X. badius collected in different places in the Notecka Forest in west-central Poland. Horizontal lines indicate: Polish (solid line) and European (dashed line) statutory limits for Cd and Pb concentrations in dried mushrooms.
M. Rudawska, T. Leski / Food Chemistry 92 (2005) 499–506
years, significant declines in the availability of certain mushrooms (chanterelles and bolets) in Poland have been observed. At the same time, the crop of X. badius increased 4-fold; 408 and 969 tons of X. badius was purchased in the years 2001 and 2002, respectively, and nearly half of them originated from the Notecka Forest (Statistical Yearbook – Forestry, 2003). Certain countries have established statutory limits for metals in edible mushrooms. In the Czech Republic, limits of 2.0 and 10.0 mg kg 1 dry matter have been established for Cd and Pb, respectively, in wild-growing mushrooms; whereas 1.0 and 10 mg kg 1 dry matter have been established for cultivated mushrooms (Kalacˇ & Svoboda, 2000). In Poland, recommendations concerning the concentrations of Cd and Pb in dried mushrooms are slightly different. The tolerance limits set for Cd and Pb are 1.0 and 2.0 mg kg 1 dry weight, respectively (Dziennik Ustaw, No. 9, position 72, 2001). The maximum level for certain contaminants in foodstuffs established by the Commission of the European Communities (Commission Regulation [EC] No 466/ 2001) is set at about 0.2 and 0.3 mg kg 1 wet weight for Cd and Pb, respectively, in cultivated fungi. Assuming that the dry matter content of mushrooms is 10% (Kalacˇ & Svoboda, 2000), these same limits for dry material will be ten times higher and approach 2.0 and 3.0 mg kg 1 dry weight for Cd and Pb, respectively. In Fig. 2(a) and (b) the range of Cd and Pb contents in caps and stipes of individual samples (n = 10) of X. badius collected in different places in the Notecka Forest are shown in relation to the statutory limits of Poland and the European Community. The results showed that most samples of X. badius from the Notecka Forest had elevated Pb concentrations (mean: 5.4 mg kg 1) and exceeded both the Polish and European tolerance limits set for dried mushrooms (Fig. 2(b)). The cadmium content in most fruiting bodies of X. badius was higher than the Polish limits, but below European statutory limits (Fig. 2(a)). The significance to human health of the element concentrations found in fruiting bodies of edible fungi may also be assessed by comparing estimated exposures with exposures from a normal diet and with the internationally agreed exposure guidelines, where these exist. These guidelines are the Provisional Tolerable Weekly Intakes (PTWIs) or Provisional Maximum Tolerable Daily Intakes (PMTDIs) set by the Joint Expert Committee on Food Additives (JECFA) of the Food and Agriculture Organization of the United Nations and the World Health Organization (FAO/WHO, 1989). Acceptable weekly intakes of Cd and Pb for adults are 0.42–0.49 and 1.5–1.75 mg, respectively. For calculations, usually 300 g of fresh mushrooms per meal is assumed (Kalacˇ & Svoboda, 2000). In relation to FAO/WHO guidelines, the PTWI for Cd is exceeded in the case of X. chrysenteron
505
(2.1-fold), A. rubescens (2.0-fold), and X. badius (1.4-fold) and for lead only in case of L. rufus (1.6-fold). Consumption of mushrooms during the harvest season is very often much higher than 300 g of fresh weight/person/week. The estimated dietary exposures to Pb and Cd by consumers of mushrooms from the Notecka Forest may exceed the appropriate guidelines on safe exposures and, therefore, mushrooms should be consumed with caution.
Acknowledgements We appreciate the technical assistance of Halina Narozna and Malgorzata Luczak. We also thank Dr. Mark Tjoelker for thoughtful reading of the manuscript and English correction. The authors also appreciate the critical comments made by the referee.
References Abuzinadah, R. A., & Read, D. J. (1986). The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. I. Utilization of peptides and proteins by ectomycorrhizal fungi. New Phytologist, 103, 481–493. Abuzinadah, R. A., & Read, D. J. (1989a). The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. IV. The utilization of peptides by birch (Betula pendula L.) infected with different mycorrhizal fungi. New Phytologist, 112, 55–60. Abuzinadah, R. A., & Read, D. J. (1989b). The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. V. Nitrogen transfer in birch (Betula pendula) grown in association with mycorrhizal and non-mycorrhizal fungi. New Phytologist, 112, 61–68. Aletor, V. A. (1985). Compositional studies on edible tropical species of mushrooms. Food Chemistry, 54, 265–268. Alofe, F. V., Odeyemi, O., & Oke, O. L. (1996). Three edible wild mushroom from Nigeria: Their proximate and mineral composition. Plant Foods for Human Nutrition, 49, 63–73. Alonso, J., Garcia, M. A., Pe´rez-Lo´pez, M., & Melgar, M. J. (2003). The concentration and bioconcentration factors of copper and zinc in edible mushrooms. Archives of Environmental Contamination and Toxicology, 44, 180–188. Aruguete, D. M., Aldstadt, J. H., & Mueller, G. M. (1998). Accumulation of several heavy metals and lanthanides in mushrooms (Agaricales) from the Chicago region. The Science of the Total Environment, 224, 43–56. Babich, H., & Stotzky, G. (1980). Environmental factors that influence the toxicity of heavy metal and gaseous pollutants to micoorganisms. Critical Reviews of Microbiology, 8, 99–145. Commission Regulation (EC) No 466/2001 of 8 March 2001 setting maximum levels of certain contaminants in foodstuffs. Official Journal of the European Communities, 16.3.2001. L77/1-13. Demirbasß, A. (2000). Accumulation of heavy metals in some edible mushrooms from Turkey. Food Chemistry, 68, 415–419. Dı´ez, V. A., & Alvarez, A. (2001). Compositional and nutritional studies on two wild edible mushrooms from northwest Spain. Food Chemistry, 75, 417–422. Dziennik Ustaw, No 9, position 72, Warsaw, Poland, 2001. FAO/WHO. (1989). Evaluation of certain food additives and contaminants, 33. Report of the Joint FAO/WHO. WHO Technical Report Series 776.
506
M. Rudawska, T. Leski / Food Chemistry 92 (2005) 499–506
Falandysz, J., Danisiewicz, D., & Bona, H. (1994). Metals content of wild growing mushrooms gathered in the Tucholskie and Kaszuby Forests. Bromatologia i Chemia Toksylogiczna, 2, 135–139. Falandysz, J., Szymczyk, K., Ichihashi, H., Bielawski, L., Gucia, M., Frankowska, A., et al. (2001). ICP/MS and ICP/AES elemental analysis (38 elements) of edible wild mushrooms growing in Poland. Food Additives and Contaminants, 6, 503–513. Falandysz, J., Lipka, K., Gucia, M., Kawano, M., Strumnik, K., & Kannan, K. (2002). Accumulation factors of mercury in mushrooms from Zaborski Landscape Park, Poland. Environment International, 28, 421–427. Fogel, R. (1976). Ecological studies of hypogeous fungi. II. Sporocarp phenology in a western Oregon Douglas Fir stand. Canadian Journal of Botany, 54, 1152–1162. Gadd, G. M. (1993). Interactions of fungi with toxic metals. New Phytologist, 124, 25–60. Gadd, G. M., & Griffiths, A. J. (1978). Microorganisms and heavy metal toxicity. Microbial Ecology, 4, 303–317. Gast, C. H., Jansen, E., Bierling, J., & Haanstra, L. (1988). Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere, 17, 789–799. Grzybek, J., & Janczy, B. (1990). Quantitative estimation of lead, cadmium, and nickel content by means of Atomic Absorption Spectroscopy in fruit bodies of some macromycetes in Poland. Acta Mycologica, 26, 17–23. Harmon, M. E., Sexton, J., Caldwell, B. A., & Carpenter, S. E. (1994). Fungal sporocarp mediated losses of Ca, Fe, K, Mg, Mn, N, P and Zn from conifer logs in the early stages of decomposition. Canadian Journal of Forerest Research, 24, 1883–1893. Kabata-Pendias, A., & Pendias, H. (1999). Biogeochemistry of trace elements. Warsaw: PWN. Kalacˇ, P., & Svoboda, L. A. (2000). Review of trace element concentrations in edible mushrooms. Food Chemistry, 62, 273–281. Kreula, M., Saarivirta, M., & Karanko, S.-L. (1976). On the composition of nutrients in wild and cultivated mushrooms. Karstenia, 16, 10–14. Latiff, L. A., Daran, A. B. M., & Mohamed, A. B. (1996). Relative distribution of minerals in the pileus and stalk of some selected edible mushrooms. Food Chemistry, 56, 115–121. Longvah, T., & Deosthale, Y. G. (1998). Compositional and nutritional studies on edible wild mushroom from northeast India. Food Chemistry, 63, 331–334. Malinowska, E., Szafer, P., & Falandysz, J. (2004). Metals bioaccumulation by bay bolete, Xerocomus badius, from selected sites in Poland. Food Chemistry, 84, 405–416. Manzi, P., Aguzzi, A., & Pizzoferrato, L. (2001). Nutritional value of mushrooms widely consumed in Italy. Food Chemistry, 73, 321–325. Manzi, P., Gambelli, L., Marconi, S., Vivanti, V., & Pizzoferrato, L. (1999). Nutrients in edible mushrooms: an inter-species comparative study. Food Chemistry, 65, 477–482. Ohtonen, R. (1986). The effect of forest fertilization on the nitrogen content of the fruit-bodies of two mycorrhizal fungi, Lactarius
rufus and Suillus variegatus. Annales Botanici Fennici, 23, 189–203. Oleksyn, J., Reich, P. B., Karolewski, P., Tjoelker, M. G., & Chalupka, W. (1999). Nutritional status of pollen and needles of diverse Pinus sylvestris populations grown at sites with contrasting pollution. Water Air and Soil Pollution, 110, 195–212. Oleksyn, J., Reich, P. B., Zytkowiak, R., Karolewski, P., & Tjoelker, M. G. (2002). Needle nutrients in geographically diverse Pinus sylvestris L. populations. Annals of Forest Science, 59, 1–18. Perez-Moreno, J., & Read, D. J. (2000). Mobilization and transfer of nutrients from litter to tree seedlings via the vegetative mycelium of ectomycorrhizal plants. New Phytologist, 145, 301–309. Reich, P. B., Oleksyn, J., & Tjoelker, M. G. (1994). Relationship of aluminium and calcium to net CO2 exchange among diverse Scots pine provenances under pollution stress in Polanad. Oecologia, 97, 82–92. Rudawska, M., Kieliszewska-Rokicka, B., Leski, T., & Oleksyn, J. (1995). Mycorrhizal status of a Scots pine (Pinus sylvestris L.) plantation affected by pollution from a phosphate fertilizer plant. Water Air and Soil Pollution, 85, 1281–1286. Ru¨hling, A., & So¨derstro¨m, B. (1990). Changes in fruitbodies production of mycorrhizal and litter decomposing macromycetes in heavy metal polluted coniferous forest in North Sweden. Water Air and Soil Pollution, 49, 375–387. Sanmee, R., Dell, B., Lumyong, P., Izumori, K., & Lumyong, S. (2003). Nutritive value of popular wild edible mushrooms from northern Thailand. Food Chemistry, 82, 527–532. Senatore, F., Dini, A., & Marino, A. (1988). Chemical constituents of some basidiomycetes. Journal of Science of Food and Agriculture, 45, 337–345. Schmitt, J. A., & Meisch, H. U. (1985). Cadmium in mushrooms, distribution growth effects and binding. Trace Elements in Medicine, 2, 163–166. Smith, S. E., & Read, D. J. (1997). Mycorrhizal symbiosis (2nd ed.). Academic Press. Statistical Yearbook – Forestry. (2003). Warsaw: Central Statistical Office. Tshinyangu, K. K. (1996). Effect of grass hay substrate on nutritional value of Pleurotus ostreatus var. colombinus. Die Nahrung, 40, 79–83. Turnau, K. (1991). The influence of cadmium dust on fungi in a PinoQuercetum forest. Ekologia Polska, 39, 39–57. Tyler, G. (1980). Metals in sporophores of basidiomycetes. Transactions of the British Mycological Society, 74, 41–49. Uggla, H., & Uggla, Z. (1979). Forest pedology (in polish). Warsaw: PWRiL. Vetter, J. (1993). Toxic elements in certain higher fungi. Food Chemistry, 48, 207–208. Vogt, K. A., & Edmonds, R. L. (1980). Patterns of nutrient concentration in basidiocarps in western Washington. Canadian Journal of Botany, 58, 694–698.